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Dunne was born in Hartford, Connecticut, and was a younger brother of author Dominick Dunne. He was the son of Dorothy Frances (née Burns) and Richard Edwin Dunne, a hospital chief of staff and prominent heart surgeon.[3][4] With several siblings, he grew up in a large, wealthy Irish Catholic family. Their maternal grandfather Dominick Francis Burns had founded the Park Street Trust Company.[5]

He started working as a journalist in New York City for Time magazine. He credited the political essayist Noel Parmentel with being his mentor in many ways.

In the late 1950s, he met Joan Didion in New York City, where she was an editor at Vogue. In a 2005 interview Didion recalled, "We amused each other and I thought he was smart. He knew a lot of stuff that I didn't know, like politics and history - I had managed to go through school without learning much except a lot of poems."[6] He invited her to travel to Connecticut one weekend in 1963 to visit his family: New England Irish Catholic, with six children. Didion said she "liked the set-up, liked being there, and liked him."[6]

They married on January 30, 1964, at Mission San Juan Bautista in California. He was 31 and she 29. They moved to a remote house on the California coast; Didion worked on a novel to follow her debut Run, River, and Dunne worked on a book about the California grape pickers' strike. They wrote a joint by-lined column for the Saturday Evening Post magazine for years. Unable to have children, in 1966 they adopted a baby at birth and named her Quintana Roo, after the Mexican state.[6]

Dunne and Didion gradually picked up writing work from book publishers and magazines, travelled together on journalism assignments, and established a working pattern that served for the next 40 years. They had a constant advising, consulting and editing collaboration. Critically acclaimed bestselling books followed for each - including for Dunne, The Studio, his non-fiction account of 20th Century Fox.

He wrote several novels, among them True Confessions, based loosely on the Black Dahlia murder, and Dutch Shea, Jr.. He was the writer and narrator of the 1990 PBS documentary L.A. is It with John Gregory Dunne, in which he guided viewers through the cultural landscape of Los Angeles.

Dunne and Didion moved to Manhattan. He died there of a heart attack in December 2003.[7] His final novel, Nothing Lost, which was in galleys at the time of his death, was published in 2004.